Euryhalinity is present in diverse aquatic taxa and requires flexible osmoregulation to field the challenges posed by differing salinities. Na+, K+-ATPase (NKA) is a ubiquitous ion pump in the gills of fishes and, for some species, paralogs of the catalytic α-subunit (NKA α1a and α1b) exhibit reciprocal expression between fresh- and seawater, termed paralog-switching. We investigated the expression and evolution of NKA paralogs in Alewife (Alosa pseudoharengus), a euryhaline and migratory fish. Comparisons between landlocked and diadromous life history forms and migrant and pre-migrant ontogenetic stages were used to study shifts in NKA paralog expression related to freshwater or seawater specialization. We exposed juvenile diadromous and landlocked alewives to freshwater (0 ppt) and seawater (30 ppt) for 2, 5, and 15 days. Additionally, we sampled migrant and pre-migrant alewives from the natal freshwater environment or after 24 hours in seawater. Diadromous Alewife exhibited salinity-dependent paralog switching, and the freshwater-specialized landlocked life history form showed greater upregulation of NKA α1b in seawater. Migrant Alewife showed a loss of freshwater readiness traded for seawater specialization through greater reliance (via upregulation) on NKA α1a in freshwater. Molecular phylogenies show Alewife NKA paralogs originated independently of paralogs in salmonids and other members of Euteleosteomorpha. This study demonstrated that NKA paralog switching is tied to halohabitat profile and that duplications of the ancestral NKA gene provided the substrate for multiple, independent molecular solutions for supporting a diadromous life history.